Exonuclease hDIS3L2 specifies an exosome-independent 3′-5′ degradation pathway of human cytoplasmic mRNA

EMBO Journal

Volumn 32, Issue 13, 2013, Pages 1855-1868

  Lubas, Michal ^a,b,c   Damgaard, Christian K ^a   Tomecki, Rafal ^b,c   Cysewski, Dominik ^b,c   Jensen, Torben Heick ^a   Dziembowski, Andrzej ^b,c  

^a AARHUS UNIVERSITY   (Denmark)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c UNIVERSITY OF WARSAW   (Poland)

Author keywords

Hdis3l2; P bodies; Ribonuclease; Rna decay; Xrn1

Indexed keywords

EXONUCLEASE; EXORIBONUCLEASE; MESSENGER RNA;

ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; EXOSOME; FEMALE; GENE ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; RNA METABOLISM; RNA PROCESSING; RNA SEQUENCE;

BLOTTING, NORTHERN; CYTOPLASM; EXORIBONUCLEASES; EXOSOME MULTIENZYME RIBONUCLEASE COMPLEX; EXOSOMES; HELA CELLS; HUMANS; MICROBODIES; MICROTUBULE-ASSOCIATED PROTEINS; POLYRIBOSOMES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84880224541     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.135     Document Type: Article

References (69)

1. Allalou A, Wahlby C (2009) BlobFinder, a tool for fluorescence microscopy image cytometry. Comput Methods Prog Biomed 94: 58-65
2. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410
3. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106
4. Anderson JS, Parker RP (1998) The 30 to 50 degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 30 to 50 exonucleases of the exosome complex. EMBO J 17: 1497-1506
5. Astuti D, Morris MR, Cooper WN, Staals RH, Wake NC, Fews GA, Gill H, Gentle D, Shuib S, Ricketts CJ, Cole T, van Essen AJ, van Lingen RA, Neri G, Opitz JM, Rump P, Stolte-Dijkstra I, Muller F, Pruijn GJ, Latif F et al (2012) Germline mutations in DIS3L2 cause the Perlman syndrome of overgrowth and Wilms tumor susceptibility. Nat Genet 44: 277-284
6. Bakheet T, Williams BR, Khabar KS (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34: D111-D114
7. Balagopal V, Fluch L, Nissan T (2012) Ways and means of eukaryotic mRNA decay. Biochim Biophys Acta 1819: 593-603
8. Bonneau F, Basquin J, Ebert J, Lorentzen E, Conti E (2009) The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell 139: 547-559
9. Chang HM, Triboulet R, Thornton JE, Gregory RI (2013) A role for the Perlman syndrome exonuclease Dis3l2 in the Lin28-let-7 pathway. Nature 497: 244-248
10. Chen CY, Gherzi R, Ong SE, Chan EL, Raijmakers R, Pruijn GJ, Stoecklin G, Moroni C, Mann M, Karin M (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107: 451-464
11. Chen CY, Shyu AB (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20: 465-470
12. Cheng ZF, Deutscher MP (2002) Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J Biol Chem 277: 21624-21629
13. Cougot N, Babajko S, Seraphin B (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165: 31-40
14. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372
15. Damgaard CK, Lykke-Andersen J (2011) Translational coregulation of 50TOP mRNAs by TIA-1 and TIAR. Genes Dev 25: 2057-2068
16. Decker CJ, Parker R (1993) A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev 7: 1632-1643
17. Decker CJ, Parker R (2012) P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol 4: a012286
18. Dolken L, Ruzsics Z, Radle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P, Koszinowski UH (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14: 1959-1972
19. Drazkowska K, Tomecki R, Stodus K, Kowalska K, Czarnocki-Cieciura M, Dziembowski A (2013) The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res 41: 3845-3858
20. Dziembowski A, Lorentzen E, Conti E, Seraphin B (2007) A single subunit, Dis3, is essentially responsible for yeast exosome core activity. Nat Struct Mol Biol 14: 15-22
21. Eulalio A, Rehwinkel J, Stricker M, Huntzinger E, Yang SF, Doerks T, Dorner S, Bork P, Boutros M, Izaurralde E (2007) Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev 21: 2558-2570
22. Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5 c. Distributed by the author. Seattle, WA, USA: Department of Genetics, University of Washington
23. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J (2005) Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 20: 905-915
24. Franks TM, Lykke-Andersen J (2007) TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev 21: 719-735
25. Franks TM, Lykke-Andersen J (2008) The control of mRNA decapping and P-body formation. Mol Cell 32: 605-615
26. Geisler S, Coller J (2012) Chapter Five-XRN1: a major 50 to 30 exoribonuclease in eukaryotic cells. In The Enzymes, Vol. 31, pp 97-114. NY, USA: Academic Press
27. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, Miller W, Kent WJ, Nekrutenko A (2005) Galaxy: a platform for interactive largescale genome analysis. Genome Res 15: 1451-1455
28. Goldstrohm AC, Wickens M (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat Rev Mol Cell Biol 9: 337-344
29. Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10: 356
30. Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136: 763-776
31. Hsu CL, Stevens A (1993) Yeast cells lacking 50-430 exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5' cap structure. Mol Cell Biol 13: 4826-4835
32. Hu W, Petzold C, Coller J, Baker KE (2010) Nonsense-mediated mRNA decapping occurs on polyribosomes in Saccharomyces cerevisiae. Nat Struct Mol Biol 17: 244-247
33. Hu W, Sweet TJ, Chamnongpol S, Baker KE, Coller J (2009) Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461: 225-229
34. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
35. Johnson AW, Kolodner RD (1995) Synthetic lethality of sep1 (xrn1) ski2 and sep1 (xrn1) ski3 mutants of Saccharomyces cerevisiae is independent of killer virus and suggests a general role for these genes in translation control. Mol Cell Biol 15: 2719-2727
36. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, Scheuner D, Kaufman RJ, Golan DE, Anderson P (2005) Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 169: 871-884
37. Korner CG, Wahle E (1997) Poly(A) tail shortening by a mammalian poly(A)-specific 30-exoribonuclease. J Biol Chem 272: 10448-10456
38. Lebreton A, Tomecki R, Dziembowski A, Seraphin B (2008) Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature 456: 993-996
39. Lee G, Bratkowski MA, Ding F, Ke A, Ha T (2012) Elastic coupling between RNA degradation and unwinding by an exoribonuclease. Science 336: 1726-1729
40. Lorentzen E, Basquin J, Tomecki R, Dziembowski A, Conti E (2008) Structure of the active subunit of the yeast exosome core, Rrp44: diverse modes of substrate recruitment in the RNase II nuclease family. Mol Cell 29: 717-728
41. Lubas M, Chlebowski A, Dziembowski A, Jensen TH (2012) Chapter One-Biochemistry and function of RNA exosomes. In The Enzymes, Vol. 31, pp 1-30. NY, USA: Academic Press
42. Lubas M, ChristensenMS, KristiansenMS, Domanski M, Falkenby LG, Lykke-Andersen S, Andersen JS, Dziembowski A, Jensen TH (2011) Interaction profiling identifies the human nuclear exosome targeting complex. Mol Cell 43: 624-637
43. Lykke-Andersen J, Shu MD, Steitz JA (2000) Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103: 1121-1131
44. Lykke-Andersen J, Wagner E (2005) Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev 19: 351-361
45. Lykke-Andersen S, Tomecki R, Jensen TH, Dziembowski A (2011) The eukaryotic RNA exosome: same scaffold but variable catalytic subunits. RNA Biol 8: 61-66
46. Makino DL, Baumgartner M, Conti E (2013) Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature 495: 70-75
47. Malecki M, Viegas SC, Carneiro T, Golik P, Dressaire C, Ferreira MG, Arraiano CM (2013) The exoribonuclease Dis3L2 defines a novel eukaryotic RNA degradation pathway. EMBO J 32: 1842-1854
48. Mangus DA, Jacobson A (1999) Linking mRNA turnover and translation: assessing the polyribosomal association of mRNA decay factors and degradative intermediates. Methods 17: 28-37
49. Mitchell P, Petfalski E, Shevchenko A, Mann M, Tollervey D (1997) The exosome: a conserved eukaryotic RNA processing complex containing multiple 30-450 exoribonucleases. Cell 91: 457-466
50. Muhlemann O, Jensen TH (2012) mRNP quality control goes regulatory. Trends Genet 28: 70-77
51. Muhlrad D, Decker CJ, Parker R (1994) Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 50-430 digestion of the transcript. Genes Dev 8: 855-866
52. Pei J, Tang M, Grishin NV (2008) PROMALS3D web server for accurate multiple protein sequence and structure alignments. Nucleic Acids Res 36: W30-W34
53. Sambrook J, Russell D (2001) Molecular Cloning: A Laboratory Manual. 3rd edn, Plainview, New York: Cold Spring Harbor Laboratories
54. Schaeffer D, Reis FP, Johnson SJ, Arraiano CM, van Hoof A (2012) The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Res 40: 9298-9307
55. Schaeffer D, Tsanova B, Barbas A, Reis FP, Dastidar EG, Sanchez-Rotunno M, Arraiano CM, van Hoof A (2009) The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities. Nat Struct Mol Biol 16: 56-62
56. Schilders G, van Dijk E, Pruijn GJ (2007) C1D and hMtr4p associate with the human exosome subunit PM/Scl-100 and are involved in pre-rRNA processing. Nucleic Acids Res 35: 2564-2572
57. Schneider C, Leung E, Brown J, Tollervey D (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37: 1127-1140
58. Schoenberg DR, Maquat LE (2012) Regulation of cytoplasmic mRNA decay. Nat Rev Genet 13: 246-259
59. Sheth U, Parker R (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805-808
60. Staals RH, Bronkhorst AW, Schilders G, Slomovic S, Schuster G, Heck AJ, Raijmakers R, Pruijn GJ (2010) Dis3-like 1: a novel exoribonuclease associated with the human exosome. EMBO J 29: 2358-2367
61. Stevens A (1980) Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 5'-mononucleotides by a 50 leads to 30 mode of hydrolysis. J Biol Chem 255: 3080-3085
62. Stoecklin G, Mayo T, Anderson P (2006) ARE-mRNA degradation requires the 50-30 decay pathway. EMBO Rep 7: 72-77
63. Tomecki R, Kristiansen MS, Lykke-Andersen S, Chlebowski A, Larsen KM, Szczesny RJ, Drazkowska K, Pastula A, Andersen JS, Stepien PP, Dziembowski A, Jensen TH (2010) The human core exosome interacts with differentially localized processive RNases: hDIS3 and hDIS3L. EMBO J 29: 2342-2357
64. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111
65. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R (2001) The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104: 377-386
66. Wang Z, Jiao X, Carr-Schmid A, Kiledjian M (2002) The hDcp2 protein is a mammalian mRNA decapping enzyme. Proc Natl Acad Sci USA 99: 12663-12668
67. Wasmuth EV, Lima CD (2012) Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol Cell 48: 133-144
68. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191
69. Zhang W, Murphy C, Sieburth LE (2010) Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc Natl Acad Sci USA 107: 15981-15985